ICTV Virus Taxonomy Profile: Closteroviridae Marc Fuchs, Moshe Bar-Joseph, Thierry Candresse, Hans Maree, Giovanni Martelli, Michael Melzer, Wulf Menzel, Angelantonio Minafra, Sead Sabanadzovic, Ictv Report Consortium

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Marc Fuchs, Moshe Bar-Joseph, Thierry Candresse, Hans Maree, Giovanni Martelli, et al.. ICTV Virus Taxonomy Profile: Closteroviridae. Journal of General Virology, Microbiology Society, 2020, 101, pp.364 - 365. ￿10.1099/jgv.0.001397￿. ￿hal-02562393￿

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Distributed under a Creative Commons Attribution| 4.0 International License ICTV VIRUS TAXONOMY PROFILE Fuchs et al., Journal of General Virology 2020;101:364–365 DOI 10.1099/jgv.0.001397 ICTV

ICTV Virus Taxonomy Profile: Closteroviridae

Marc Fuchs1,*, Moshe Bar-Joseph­ 2, Thierry Candresse3, Hans J. Maree4, Giovanni P. Martelli5†, Michael J. Melzer6, Wulf Menzel7, Angelantonio Minafra5, Sead Sabanadzovic8 and ICTV Report Consortium

Abstract Viruses in the family Closteroviridae have a mono-, bi- or tripartite positive-sense­ RNA genome of 13–19 kb, and non-enveloped,­ filamentous particles 650–2200 nm long and 12 nm in diameter. They infect plants, mainly dicots, many of which are fruit crops. This is a summary of the ICTV Report on the family Closteroviridae, which is available at ictv.​ global/​ report/​ closteroviridae​ .

Table 1. Characteristics of members of the family Closteroviridae

Typical member: citrus tristeza virus (U16304), species Citrus tristeza virus, genus Closterovirus

Virion Non-­enveloped, filamentous particles 650 to 2200 nm in length and 12 nm in diameter

Genome 13–19 kb of positive-­sense, mono-, bi- or tripartite RNA

Replication In association with endoplasmic reticulum-­derived membranous vesicles and vesiculated mitochondria

Translation Directly from genomic RNAs as large polyproteins or from sub-­genomic mRNAs

Host range Plants (mainly dicots), transmitted by aphids, whiteflies, mealybugs or soft-scale­ insects. No seed or pollen transmission

Taxonomy Realm Riboviria, four genera, more than 50 species, some unassigned to a genus

VIRION GENOME Virions are long, helically constructed filamentous particles; The genome consists of 1–3 molecules of 5′-capped, linear, positive-­sense RNA that lack a 3′-terminal poly(A) or tRNA-like­ the primary helix has a pitch of 3.4–3.8 nm, about 10 protein structure (Fig. 2). The genome organization is conserved; the subunits per turn and a central hole of 3–4 nm (Table 1). number and relative position of open reading frames (ORFs) The coat protein (CP) and minor CP (CPm) are the most can differ. The dual-­gene module ORF1a–ORF1b at the 5′-end of genomic RNA encodes replication-associated­ proteins with abundant virion components. CPm encapsidates the 600–700 conserved domains for a papain-like­ cysteine protease (l-­Pro), 5′-terminal nucleotides of viral RNA (Fig. 1). The virus-­ methyltransferase (Met), helicase (Hel) and RNA-­directed RNA encoded heat shock protein 70 homologue (HSP70h) and the polymerase (RdRP). Downstream ORFs form a conserved five-gene­ module encoding a 6K small hydrophobic protein, ∼60 kDa protein are also integral to virions; a 20 kDa protein HSP70h, a ~60 kDa protein, CP and CPm [1]. Genome expres- may form the tip of the virion head [1]. sion involves proteolytic processing of the polyprotein encoded

Received 21 January 2020; Accepted 30 January 2020; Published 05 March 2020 Author affiliations: 1School of Integrative Plant Science, Cornell University, Geneva, NY 14456, USA; 2The S. Tolkowsky Laboratory, Bet Dagan 50250, Israel; 3UMR 1332 Biologie du Fruit et Pathologie, INRA, University of Bordeaux, 33882 Bordeaux, France; 4Department of Genetics, Stellenbosh University and Citrus Research International, Stellenbosh, Western Cape, South Africa; 5Department of Soil, Plant and Food Sciences, Università degli Studi di Bari Aldo Moro, Bari, Italy; 6Department of Plant and Environmental Protection Sciences, University of Hawai’i at Manoa, Honolulu, HI 96822, USA; 7Leibniz-Institute­ DSMZ – German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany; 8Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi, MS 39762, USA. *Correspondence: Marc Fuchs, marc.​ fuchs@​ cornell.​ edu​ Keywords: Closteroviridae; ICTV Report; Taxonomy. Abbreviations: CP, coat protein; CPm, minor coat protein; Hel, helicase; HSP70h, heat shock protein 70 homolog; L-Pro,­ papain-­like cysteine protease; Met, methyltransferase; RdRP, RNA-­directed RNA polymerase. †This work is dedicated to the memory of our friend and colleague Professor Giovanni Paolo Martelli, former chair of the Study Group on Clostero- viridae and Life Member of the ICTV, who died in January 2020. 001397 © 2020 The Authors This is an open-­access article distributed under the terms of the Creative Commons Attribution License.

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transcription of sgmRNAs is temporally and quantitatively regulated, with each serving as a monocistronic messenger for translation of the corresponding 5′-proximal ORF.

TAXONOMY The genome of members of the genus Closterovirus is monopar- tite with CPm encoded upstream of CP. Transmission is by aphids in a semi-persistent­ manner [5]. Ampelovirus genomes are monopartite and show wide variation in size and organiza- tion. Transmission is by pseudococcid mealybugs and soft-­scale insects in a semi-persistent­ manner. Crinivirus genomes are bi-or­ tripartite. Transmission is by whiteflies in a semi-persistent­ Fig. 1. Electron micrographs of virions of beet yellows virus (genus manner. Viruses in these three genera have a narrow host range Closterovirus) negatively-­stained and decorated with an antiserum and wide distribution; symptoms consist of foliar discoloration specific to (a) CP (bare for the CPm tail) and (b) CPm (75 nm tail only). and deformation (yellowing, reddening, mottling, rolling), (c) as (b) for four selected particles. Scale bar 300 nm. Reproduced with stunting and pitting. Velarivirus genomes are monopartite. permission from [6]. Hemipteran vectors have not been identified; there are no apparent symptoms.

RESOURCES Current ICTV Report on the family Closteroviridae: ​ictv.​global/​ report/​closteroviridae.

Funding information Production of this summary, the online chapter, and associ- ated resources was funded by a grant from the Wellcome Trust (WT108418AIA).

Acknowledgements Members of the ICTV Report Consortium are Stuart G. Siddell, Elliot J. Lefkowitz, Andrew J. Davison, Peter Simmonds, Sead Sabanadzovic, Donald B. Smith, Richard J. Orton and F. Murilo Zerbini. Conflicts of interest The authors declare that there are no conflicts of interest.

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